Abstract
Previous restriction fragment length polymorphism analysis divided variola virus (VARV) strains into two subtypes, one of which included West African and South American isolates. This allowed a dating to be introduced for the first time in estimation of the VARV evolution rate. The results were used to analyze the molecular evolution of the total family Poxviridae. Comparisons of the known nucleotide sequences were performed for the extended conserved central genome region in 42 orthopoxvirus strains and for the eight genes of multisubunit RNA polymerase in 65 viruses belonging to various genera of the family Poxviridae. Using the Bayesian dating method, the mutation accumulation rate of poxviruses was estimated at (1.7–8.8) × 10−6 nucleotide substitutions per site per year. Computations showed that the modern poxvirus genera started diverging from an ancestral virus more than 200 thousand years ago and that an ancestor of the genus Orthopoxvirus emerged 131 ± 45 thousand years ago. The other genera of mammalian poxviruses with a low GC content diverged approximately 110–90 thousand years ago. The independent evolution of VARV started 3.4 ± 0.8 thousand years ago. It was shown with the example of VARV and the monkeypox virus (MPXV) that divergent evolution of these orthopoxviruses started and the West African subtypes of VARV and MPXV were formed as geographical conditions changed to allow isolation of West African animals from other African regions.
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Kumar, S. and Hedges, S.B., A Molecular Timescale for Vertebrate Evolution, Nature, 1998, vol. 392, pp. 917–920.
Jenkins, G.M., Rambaut, A., Pybus, O.G., and Holmes, E.C., Rates of Molecular Evolution in RNA Viruses: A Quantitative Phylogenetic Analysis, J. Mol. Evol., 2002, vol. 54, pp. 156–165.
Shackelton, L.A., Rambaut, A., Pybus, O.G., and Holmes, E.C., JC Virus Evolution and Its Association with Human Populations, J. Virol., 2006, vol. 80, pp. 9928–9933.
Fares, M.A. and Holmes, E.C., A Revised Evolutionary History of Hepatitis B Virus (HBV), J. Mol. Evol., 2002, vol. 54, pp. 807–814.
Osiowy, C., Giles, E., Tanaka, Y., et al., Molecular Evolution of Hepatitis B Virus over 25 Years, J. Virol., 2006, vol. 80, pp. 10 307–10 314.
Girones, R. and Miller, R.H., Mutation Rate of the Hepadnavirus Genome, Virology, 1989, vol. 170, pp. 595–597.
Shackelton, L.A. and Holmes, E.C., Phylogenetic Evidence for the Rapid Evolution of Human B19 Erythrovirus, J. Virol., 2006, vol. 80, pp. 3666–3669.
Shackelton, L.A., Parrish, C.R., Truyen, U., and Holmes, E.C., High Rate of Viral Evolution Associated with the Emergence of Carnivore Parvovirus, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 379–384.
Ong, C.K., Chan, S.Y., Campo, M.S., et al., Evolution of Human Papillomavirus Type 18: An Ancient Phylogenetic Root in Africa and Intratype Diversity Reflect Coevolution with Human Ethnic Groups, J. Virol., 1993, vol. 67, pp. 6424–6431.
McGeoch, D.J. and Cook, S., Molecular Phylogeny of the Alphaherpesvirinae Subfamily and a Proposed Evolutionary Timescale, J. Mol. Biol., 1994, vol. 238, pp. 9–22.
McGeoch, D.J., Cook, S., Dolan, A., et al., Molecular Phylogeny and Evolutionary Timescale for the Family of Mammalian Herpesviruses, J. Mol. Biol., 1995, vol. 247, pp. 443–458.
Bowden, R., Sakaoka, H., Ward, R., and Donnelly, P., Patterns of Eurasian HSV-1 Molecular Diversity and Inferences of Human Migrations, Infect. Genet. Evol., 2006, vol. 6, pp. 63–74.
Bernard, H.U., Coevolution of Papillomaviruses with Human Populations, Trends Microbiol., 1994, vol. 2, pp. 140–143.
Gottschling, M., Kohle, A., Stockfleth, E., and Nindl, I., Phylogenetic Analysis of β-Papillomaviruses as Inferred from Nucleotide and Amino Acid Sequence Data, Mol. Phylogenet. Evol., 2007, vol. 42, pp. 213–222.
Sugimoto, C., Hasegawa, M., Kato, A., et al., Evolution of Human Polyomavirus JC: Implications for the Population History of Humans, J. Mol. Evol., 2002, vol. 54, pp. 285–297.
Lefkowitz, E.J., Wang, C., and Upton, C., Poxviruses: Past, Present and Future, Virus Res., 2006, vol. 117, pp. 105–118.
Fenner, F., Henderson, D.A., Arita, I., et al., Smallpox and Its Eradication, Genewa: World Health Organization, 1988.
Shchelkunov, S.N., Marennikova, S.S., and Moyer, R.W., Orthopoxviruses Pathogenic for Humans, Berlin: Springer-Verlag, 2005.
Shchelkunov, S.N., Totmenin, A.V., Loparev, V.N., et al., Alastrim Smallpox Variola Minor Virus Genome DNA Sequences, Virology, 2000, vol. 266, pp. 361–386.
Babkina, I.N., Babkin, I.V., Li, Yu., et al., Phylogenetic Comparison of Genomes of Different Variola (Smallpox) Virus Strains, Dokl. Akad. Nauk, 2004, vol. 398, pp. 316–319.
Babkin, I.V. and Shchelkunov, S.N., Time Scale of Poxvirus Evolution, Mol. Biol. (Moscow), 2006, vol. 40, pp. 20–24.
Esposito, J.J., Sammons, S.A., Frace, A.M., et al., Genome Sequence Diversity and Clues to the Evolution of Variola (Smallpox) Virus, Science, 2006, vol. 313, pp. 807–812.
Thompson, J.D., Gibson, T.J., Plewniak, F., et al., The ClustalX Windows Interface: Flexible Strategies for Multiple Sequence Alignment Aided by Quality Analysis Tools, Nucleic Acids Res., 1997, vol. 24, pp. 4876–4882.
Huelsenbeck, J.P. and Rannala, B., Maximum Likelihood Estimation of Phylogeny Using Stratigraphic Data, Paleobiol., 1997, vol. 23, pp. 174–180.
Posada, D. and Crandall, K.A., Modeltest: Testing the Model of DNA Substitution, Bioinformatics, 1998, vol. 14, pp. 817–818.
Kumar, S., Tamura, K., and Nei, M., MEGA3: Integrated Software for Molecular Evolutionary Genetics Analysis and Sequence Alignment, Brief. Bioinform., 2004, vol. 5, pp. 150–163.
Tajima, F., Simple Methods for Testing the Molecular Evolutionary Clock Hypothesis, Genetics, 1993, vol. 135, pp. 599–607.
Kishino, H., Thorne, J.L., and Bruno, W.J., Performance of a Divergence Time Estimation Method under a Probabilistic Model of Rate Evolution, Mol. Biol. Evol., 2001, vol. 18, pp. 352–361.
Nei, M. and Gojobori, T., Simple Methods for Estimating the Numbers of Synonymous and Nonsynonymous Nucleotide Substitutions, Mol. Biol. Evol., 1986, vol. 3, pp. 418–426.
McLysaght, A., Baldi, P.F., and Gaut, B.S., Extensive Gene Gain Associated with Adaptive Evolution of Poxviruses, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 15655–15660.
Moss, B., Poxviridae: The Viruses and Their Replication, Fields Virology, Fields, B.N., Knipe, D.M., Howley, P.M., et al., Eds., Philadelphia: Lippincott-Raven, 1996, pp. 2637–2671.
Gubser, C. and Smith, G.L., The Sequence of Camelpox Virus Shows It Is Most Closely Related to Variola Virus, the Cause of Smallpox, J. Gen. Virol., 2002, vol. 83, pp. 855–872.
Iyer, L.M., Balaji, S., Koonin, E.V., and Aravind, L., Evolutionary Genomics of Nucleo-Cytoplasmic Large DNA Viruses, Virus Res., 2006, vol. 117, pp. 156–184.
Gubser, C., Hue, S., Kellam, P., and Smith, G.L., Poxvirus Genomes: A Phylogenetic Analysis, J. Gen. Virol., 2004, vol. 85, pp. 105–117.
Suzuki, Y. and Gojobori, T., The Origin and Evolution of Ebola and Marburg Viruses, Mol. Biol. Evol., 1997, vol. 14, pp. 800–806.
Gao, F., Yue, L., White, A.T., et al., Human Infection by Genetically Diverse SIVsm-Related HIV-2 in West Africa, Nature, 1992, vol. 358, pp. 495–499.
Simmonds, P., The Origin and Evolution of Hepatitis Viruses in Humans, J. Gen. Virol., 2001, vol. 82, pp. 693–712.
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Original Russian Text © I.V. Babkin, S.N. Shchelkunov, 2008, published in Genetika, 2008, Vol. 44, No. 8, pp. 1029–1044.
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Babkin, I.V., Shchelkunov, S.N. Molecular evolution of poxviruses. Russ J Genet 44, 895–908 (2008). https://doi.org/10.1134/S1022795408080036
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DOI: https://doi.org/10.1134/S1022795408080036